No matter how much the natural sciences lay claim to a direct access to phenomena, this access will always have to be articulated in a language defined by cultural norms and traditions (Gullestad 2011).

Parasite ecology research has taken off since the 1970s (Raffel et al. 2008; Moore 2012; Lively et al. 2014; Poulin 2021; but see Preston et al. 2016; Andrew et al. 2021). Many factors explain the rapid shifts in the field, including the development of key mathematical models (e.g., Anderson and May 1978), insights from community ecology (e.g., Holmes 1973), and new genetic tools (e.g., Wickström et al. 2003). This progress has overturned some erroneous hypotheses about parasites, including (1) that they are degenerate and simplified creatures; (2) that they do not play important roles in regulating ecosystem dynamics or shaping food webs; and (3) that parasites only weakly influence their hosts’ evolution, population dynamics, and behavior (among others; see Mittelbach 2005; Vickerman 2009; Moore 2012; Poulin 2021).

Strikingly, such mistaken assumptions about the ecology of parasites of animal hosts (hereafter, animal parasites) appear to have been more pervasive and fundamental than in related fields, such as predator-prey ecology, resulting in a prolonged period of parasite exclusion from mainstream ecological research (as reviewed in Poulin 2021 and below). Additionally, parasites have continued to be misunderstood despite the progress in ecological parasitology. Just over a decade ago, for instance, it seemed reasonable for researchers to argue that “basic assumptions about parasites, their ubiquity, and their relevance need to be reexamined or abandoned” (Gómez and Nichols 2013, 225). More recently, researchers have claimed that parasites are still being neglected, contending that “their omission from the design and analyses of ecological studies poses real risks of flawed interpretations” (Timi and Poulin 2020, 759).

This situation raises two questions. First, what explains the accumulation of so many erroneous assumptions about animal parasites? Secondly, why have some of these assumptions lingered long after there was ample evidence against them?

Complete answers to these questions will cite many factors. Animal parasites are, of course, small and difficult to study in their natural environments (frequently, inside their hosts). And before the takeoff of ecological parasitology, researchers lacked many of the tools that are now regarded as essential to understanding parasites properly. So, it may not be surprising that earlier generations of scientists had poor models of these organisms and their ecological significance. Moreover, it takes time for scientific developments to be disseminated and fully integrated into subsequent work; so, it may not be surprising that certain errors persist decades after they are known to be errors.

While these are, no doubt, central parts of the story, our aim here is to argue for the importance of another component. As Reynolds (2018, 2) argues, the metaphors that scientists adopt “can be integral to the formulation of a theory and constitute the core of action-guiding programs of research. They also incorporate implicit value judgments about the nature of the subject matter under investigation and the proper route to its scientific understanding.” And “parasite” is itself a metaphor, a piece of language originally applied to humans that was co-opted for scientific use (as we’ll discuss below). We argue that the negative cultural perceptions of parasites caused a range of negative associations with the term “parasite” and its cognates, even for scientists who study these organisms, and that these negative associations resulted in cognitive biases regarding animal parasites that influenced research priorities, the development of new explanatory frameworks, and the eventual acceptance of these frameworks.

We are hardly the first to note the prevalence of erroneous assumptions about, and the neglect of, animal parasites in ecology (Moore 2012; Poulin 2021). However, previous authors have neither detailed the historical roots of this problem nor provided contrasting cases to bolster the hypothesis that cultural and linguistic value associations influenced the development of ecological theory. We do both here. We provide a novel comparison of the value associations for two categories of natural enemies, animal parasites and predators, that are commonly used as biological-social metaphors. After describing generally how language is known to impact the development of scientific theory, we move to exploring the case of parasites and predators by: (1) demonstrating the disparity in treatment between predators and parasites in ecological literature, (2) identifying the historical origin of the relevant value associations prior to these terms’ ecological adoption, and (3) providing two case studies that illustrate how these value associations impacted ecology. We conclude with some suggestions about how negative value associations in science might be addressed.

Scientists often borrow terminology from the broader culture to describe phenomena of interest. Often enough, the societal values associated with that language partially explain why that language is perceived to be useful, despite the ostensible desire for value neutrality in scientific discourse (e.g., Lewontin 1992, Larson 2011). One such example is the male ‘king bee’ (now queen bee), who reigned over honeybee colonies from Aristotle’s 350 B.C.E. History of Animals to Hyll’s 1579 beekeeping manual. Western philosopher-scientists adopted the term ‘king’ to describe the sex and social position of the dominant bee in each colony because of their assumptions – implicit or explicit – about who has power and who can lead (Wilson 2014a). Once adopted, the term nudged scientists towards a “general orthodoxy of the king bee,” (Wilson 2014a) hampering our understanding of bee sex and social organization (Maderspacher 2007).

The (correct) alternate hypothesis existed throughout this entire period, though it was not popularized nor rigorously tested: the ‘mother’ bee is mentioned in sources as far back as Aristotle’s contemporaries, though, notably, none proposed that the female rules the colony (Maderspacher 2007; Grinnell 2016; Videen 2016). It was only following Queen Elizabeth I’s reign (1558–1603) that the first scientific works about a female queen bee circulated in England (Butler’s 1609 The Feminin’ Monarchie), though her rule did nothing to change the entanglement of bee colonies and metaphoric royalty.¹

The case of the “king bee” illustrates that cultural values can subtly inform scientific theory. If those theories become prominent, then inertia can anchor the scientific community in ways of thinking that are basically misguided (Chu and Evans 2021). There is ample evidence that background beliefs can nudge scientists in many ways, affecting how researchers allocate their attention (Rees et al. 1999), how they interpret data (Brewer and Chinn 1994), what they perceive when making observations (Gunstone and White 1981), and what they judge worth communicating in their publications (Holton 1978). This can lead to long periods during which scientists try to make existing theories compatible with recalcitrant evidence (as illustrated by astronomical epicycles; Gingerich 1993) or simply miss such evidence entirely (as in the study of the evolution of the female orgasm; Lloyd 2006).

Early ecologists provide another example of cultural values informing theory, though the consequences are more complicated. When Haeckel, for instance, defined ecology as “the economy of nature” in 1869 (Egerton 2013), that phrase no longer meant something like “the order of nature,” as it had in the pre-Darwinian period. Instead, it was now informed directly by Darwin’s 1859 Origin of Species, which systematically employs economic concepts in the theory of natural selection – competition, the division of labor, scarcity of resources, and so on – borrowed from the likes of Adam Smith and Thomas Malthus. And just as economies were thought to tend toward stable equilibria, regulated by the “invisible hand” that emerges when all actors pursue their own self-interest, Haeckel thought that ecological systems did too: such systems are governed by the “balance of nature,” where “the absolute number of organic individuals populating our world … remain[s] constant, and … only the relative numbers of the individual species … alter continually in relation to each other” (quoted in Egerton 2013, 227). Earlier biologists had understood the “balance of nature” in religious terms, attributing homeostasis to the divine ordering of the natural world. The economic view of ecological systems allowed scientists to preserve a sense of the correctness of that order without positing supernatural action. This may well have delayed scientists’ appreciation of nature’s stochasticity, not to mention many objectionable uses of the theory of natural selection to prop up certain hegemonic (power-structured and dominance-maintaining) human institutions.

These examples do not show that it is inherently objectionable to use value-laden language for scientific purposes. Instead, they illustrate the importance of thinking systematically about when and why to co-opt value-laden language for scientific purposes. In any case, our focus here is on one particular context where value-laden language had impacts on science. As mentioned earlier, we’ll explore this issue by contrasting the cases of parasites and predators. Despite ecologists’ appreciating that parasites and predators are similar in important respects, they paid parasites much less attention than predators and understood their ecological traits quite differently. Again, we do not want to suggest that values associated with parasites and parasitism were the only or even primary factors in this neglect, only that history suggests that they had some important role to play.

Though obviously different in many respects (Lafferty and Kuris 2002; Raffel et al. 2008), parasitism and predation share characteristics common to all consumer-resource interactions (Thomas et al. 2005b; Hall 2008). Early ecologists explicitly acknowledged this similarity – Elton (1927, 75) wrote, “it is best to treat parasites as being essentially the same as carnivores” – and other prominent ecologists have continued to associate parasites and predators (Hairston et al. 1960; Janzen 1970; Wilson 2014b). Notably, parasites were not completely ignored by all biological disciplines, such as taxonomy (“old school natural history”; Poulin 2021, 1073). Moreover, in part because parasites were targeted for eradication due to their impacts on the economy and human health (Cox 2002), parasitologists themselves began asking ecological questions about parasites long before ecologists began to seriously consider parasites as important players in ecological communities (e.g., Farley 2003; Worboys 1983). Still, it remains the case that animal parasites were at the margins of ecology throughout its early history (Jackson 2015).

This disparity in ecological research priority was apparent early in the 20th century. When reviewing recent progress in food cycles, Lindeman (1942, 405) wrote that “the various categories of parasites are somewhat comparable to those of the predators, but the details of [parasites’] energy relationships have not yet been clarified, and cannot be included.” This may be due to untested assumptions about the roles of (weak) parasites and (powerful) predators in controlling other species (about which we’ll have more to say later). Muir (Williams 1931, 26), for instance, stated that “theoretically, other things being equal, a predator should be more valuable [read: influential] than a parasite” and Elton (1927, 81) stated that “in [the food cycles of] an animal community … parasites do not play a very important part” – without providing evidence for the claim. By comparison, the introduction of a review by Errington in 1946 suggested that studies of predation “surely number in the many thousands of titles…. Whatever else may be said of predation, it does draw attention” (144).

The disparity grew as mid-to-late-20^th century ecologists continued to demonstrate the important roles of animal predators in their ecosystems (e.g., Paine 1966; Slobodkin et al. 1967; often called ‘trophic cascades’, Paine 1980). Predators were described as “powerful” (Hutchinson 1957); “dominant” (Van Valen 1973a); “ubiquitous” (Ricklefs 1987); “major importance/regulator” (Blair 1950; Slobodkin et al. 1967); and even “keystone,” which was coined by Paine (1969a) in reference to influential, high trophic level predators before being more broadly redefined to include parasites (Power et al. 1996; Estes and Palmisano 1974). By contrast, parasites were either ignored or subsumed by predators (e.g., in Lotka-Volterra equations; Lotka 1925; Volterra 1926a, 1926b; Kingsland 2015). This systemic disparity produced an ecological literature where “competition and predation have been traditionally considered as major biotic determinants of community structure, [while] parasites have been virtually ignored” (Thomas et al. 2005a, 124).

Anderson and May’s (1978–1982) seminal models of parasite-host dynamics, drawing on the extensive predator-prey literature, began the process of integrating parasites into ecological theory in a more systematic way. As Heesterbeek and Roberts (2015) contend, while others were either pursuing highly abstract modeling or focused on understanding particular infectious agents, Anderson and May managed to model general epidemiological phenomena without losing sight of the biological mechanisms at work, which lent itself to improving decision-making in public health. Moreover, because they worked with a wide array of collaborators and students, Anderson and May created a new cohort of parasite and wildlife disease modelers who pushed parasite ecology research forward. As a result, the 1970s and 80s have been cited as the dawn of a parasite research revolution by many ecologists (Mittelbach 2005; Poulin 2007; Vickerman 2009; Moore 2012; Englund 2014; Jackson 2015; acknowledging that others played important roles as well, e.g., Hamilton 1980; Zuk 1982; Van Valen 1973b).

Nevertheless, the disparity in research priority between parasites and predators has persisted through the late 20^th and early 21^st centuries (Poulin 2021). In a study of ecological research network dynamics between 1975 and 2014, predator-prey ecology was one of the main clusters of ecological research from 1980–2014, while parasite ecology did not appear even as a sub-cluster (Réale et al. 2020). Of the 100 highest-ranked papers in ecology published between 1858 and 2014, predators featured in 45 compared to only 18 for parasites (14 of which also featured predators). The mean ranking for predator papers without parasites was 48 (published 1934–2014), including 50% of the top ten spots, while the mean ranking for parasite-only papers was 81, with only one paper in the top 50 and all published between 1978 and 1981 (Courchamp and Bradshaw, 2017).

Similarly, Loreau et al. (2005) found that the journal Ecosystems, chosen because it reflects the incorporation of parasites into theories about ecological systems and not simply their taxonomic inclusion, had not published a single paper on parasites, parasitism, or parasitoids from its founding in 1998 to the time of their publication (versus 110 hits for predat- between 1998 and 2005; our search of the same journal yielded 90 results for parasit- and 475 results for predat- between 1998 and 2023). The proportion of papers featuring parasites relative to predators in ecology journals from 1991 to 2006 showed predators featured in at least twice as many publications as parasites (Raffel et al. 2008). Broad topical treatment by ecologists is consistent with this analysis of the primary literature: 21st-century ecology textbooks still largely neglect parasites in comparison to predators, with the majority featuring parasites at less than 50% the rate of predators (Figure 1).

If early ecologists recognized the similarities between predators and parasites, why have parasites continued to be relegated to the margins as less important than predators in the development of ecological theories? To help answer this question, we should briefly review the societal associations with the terms ‘parasite’ and ‘predator’ prior to their adoption by scientists.

‘Parasite’ has almost always been associated with weakness, dependence, lack of social importance, negativity, and threatening moral depravity. Contrary to the common supposition that the social (human) parasite is modeled off the biological parasite, the word referred solely to humans for over 2,000 years. The Greek parasitos dates to the 5^th century B.C.; at that time, it referred to temple assistants receiving free meals in return for festival duties. Greek comedic playwrights molded the parasitos into a trope for the stage: irreverent flatterers dependent on free food secured at the tables of the rich. The parasitos was popularized as a unidimensional ‘type’ – overwhelmingly the punchline of jokes and often an example of unethical behavior (Gullestad 2011; Musolff 2014, 2016).

Ridicule morphed into vicious insult targeted at specific individuals both in creative (e.g., a 1665 satire about Pierre de Montmaur, Epulum parasiticum; De Smet 1996) and religious works (e.g., English Catholic scholars calling John Wycliffe “a vile heretic, a most pernicious flatterer and parasite,” Rainolds and Bruce 1593). Specific species of animal parasites (e.g., the flea) were represented as simultaneously threatening to society’s most important moral values (e.g., female virginity during the British Tudor and Victorian periods) yet individually puny/weak, often through association with socially unimportant or derided individuals (Marlowe 1592; Donne 1633; Orme 2011; Prystash 2016; Filo 2019).

‘Predator’ (meaning pillager/plunderer) appears in the 15^th century, also solely in reference to humans, with a connotative duality as divinely powerful yet morally contemptible (e.g., the disgraceful nature of the king’s predation described by 15th-century political prisoner George Ashby, Bateson 1899; and Cæser, a tyrant and ‘predator’ in 1584 Don Simonides, OED 2021). According to these authors, predators were authoritative, important male figures, generally kings and emperors ruling by a natural, divine right that justified their hostile dominance. Specific animal predator species were frequently associated with power, masculinity, wealth, and social importance (e.g., the eagle on the Roman legion standard and lions on English royal crests, among others; Mylonas 1946; Julian 2004; Hünemörder 2006; Hayes 2014; Holmes 2020). Hunting, the act of human-as-predator, was generally considered the domain of strong and able men, and in some societies became a sport associated with wealth, power, and masculinity (Goldberg 2020; some of these associations lasting to the modern era, see Littlefield 2010).

When ‘parasite’ was adopted and popularized in the scientific community in the 17^th century, the associated values and concepts such as weakness, social (e.g., system-level) unimportance, depraved moral threat, and “negatively valued metaphors of dependence” (Osborne 2017, 212) came with the term (Gullestad 2011; Musolff 2016). Ecologist Elton (1927, 75) wrote in his foundational text, Animal Ecology, that “it is common to find parasites referred to as if they were in some way more morally oblique in their habits.” The moral/functional degeneracy and negative dependence of even a free-living and familiar-looking brood parasite, via a social metaphor, can be clearly seen in the popular natural history works of Neltje Blanchan and her accounts of cowbirds:

Its marital and domestic character is thoroughly bad. Polygamous and utterly irresponsible for its offspring, this bird forms a striking contrast to other feathered neighbors, and indeed is almost an anomaly in the animal kingdom … an unnatural mother may be seen skulking about in the trees and shrubbery … selecting in a cowardly way a small nest … there leaving the hatching and care of its young to the tender mercies of some already burdened little mother … keeping with its unclean habits and unholy life and character. (Blanchan 1897, 49-50)²

As these examples illustrate, and as documented more thoroughly in the quotes by ecologists in supplementary table 1, the concepts of social unimportance, weakness, and degeneracy colored the way many early ecologists viewed parasites. These associations persisted and became common in the field despite the absence of scientific evidence for them; moreover, they proved to be surprisingly durable. For instance, Lack (1954) stresses parasites’ unimportance, Haldane (1955) critiques this claim, but MacArthur (1958) repeats Lack’s view anyway – even though MacArthur engages with Haldane’s work.

‘Predator’, by contrast, was widely adopted by scientists in the early to mid-20th century. Animal predators were valorized as naturally powerful in their own ecosystems. At the same time, they were condemned when their actions threatened humans’ safety or economic interests, and thereby the hierarchy of nature (established both through religious texts, such as the Judeo-Christian creation myth, and scientifically; Aristotle’s Scala naturae and Linnaeus’ Systema naturae; Pui-lan 1992; Clutton-Brock 1995). This duality helps explain humans’ continual “love-hate relationship with predators” (“Predators on Top” 2018). On the one hand, they have long been culled when they’ve posed any threat to human interests: consider, for instance, the US decision to slaughter wolves in the late 1800s to prevent livestock predation (Dunlap 1998). However, after such threats have been minimized, predators are valorized for their critical ecosystem roles and selected as charismatic targets for conservation and ecological restoration initiatives (Dunlap 1998; Macdonald et al. 2017).

This tension is visible, again, in the work of Blanchan (1898) who writes admiringly of “innocent birds of prey” (vii), whose “...entire structure indicates strength, ferocity, carnivorous appetite, and powerful flight, have, for their diagnostic features, strong, hooked bills...” (301) But her tone changes significantly when birds of prey threaten the anthropocentric hierarchy, writing that the chicken hawk “lives by devouring birds of so much greater value than itself that the law of the survival of the fittest should be enforced by lead until these villains, from being the commonest of their generally useful tribe, adorn museum cases only.” (314-315)

On its own, this brief survey of the history of the terms ‘parasite’ and ‘predator’ is suggestive: it would be surprising if the values associated with these terms (e.g., powerful/important vs. weak/unimportant) played no roles whatever in scientists’ thinking about parasites and predators. Like the divergent societal values associated with sex and power that promulgated the reign of the “king bee,” the divergent values associated with predators and parasites probably had some impact on scientists’ appreciation of parasites’ ecological significance. However, the impacts of these values are clearer when we consider specific assumptions about parasites. In what follows, we turn to two case studies: one about the assumption that parasites are ecologically insignificant; the other about parasites being unworthy of conservation. In each case, we argue that societal values played some role in explaining why earlier scientists opted not to explore hypotheses that framed parasites as powerful/important – and thus as ecosystem assets.

We have argued that societal values associated with the terms ‘predator’ and ‘parasite’ were uncritically imported into ecology. We contend that these values partially explain both the appeal and durability of erroneous assumptions about parasites relative to predators, even though both are ecologically similar classes of consumer organisms. The values associated with predators made it easier to appreciate their ecological importance and conservation value; by contrast, the values associated with parasites made it harder to do the same.

Of course, it is not possible to quantify exactly how much harder these values made it for ecologists to appreciate the ecological importance and conservation value of parasites. In part, this is because there is no obvious metric by which to make the comparison. For instance, we can’t show that these values set back appreciation of parasites by a specific number of years. However, we think a strong case can be made that the contributions of values associated with parasites were not entirely trivial. The first part of that case involves demonstrating that ecologists persisted in their beliefs about parasites long after ample evidence became available to contradict those beliefs. At that point, it becomes necessary to seek potential cultural explanations for belief persistence. One component of scientific culture is the values associated with the concepts that scientists employ. The rest of that case involves showing that a cultural explanation of the neglect of parasites would be inadequate were it not to cite the relevant value associations. Imagine, for example, a cultural explanation that just appealed to “within-paradigm” scientific conservatism as the mechanism for the neglect of parasites. Such an explanation would miss the mechanisms by which conservatism is implemented – e.g., particular ways of understanding parasites that are informed by values – as would other explanations that attempt to avoid this level of granularity.

In any case, insofar as the value associations hypothesis is correct, it raises two important questions. One of them concerns whether there were or are any other costs of having these values shaping parasite ecology. The second focuses on moving forward: are there ways to mitigate any impacts of negative values being associated with parasites?

It takes work to retrofit parasites into a century of ecological research that ignored them; in some cases, it is difficult enough that some researchers have argued that we must start anew (e.g. food web theory; Sukhdeo 2010). Moreover, when societal values are uncritically incorporated into scientific theories, they can lend themselves to unfortunate social uses. Credit is due to the many researchers who have questioned prevailing societal and cognitive biases about roles of parasites in ecological systems when confronted with contradictory evidence. However, it would have been far better – for researchers, for conservation, and for parasites themselves – had earlier generations of ecologists been more aware, more reflective, and more critical of the values that informed the way these organisms were viewed and studied.

Scientists have some responsibility to be critical of the concepts they borrow and question the values associated with them. This process can be facilitated by reconfiguring our conception of the relationship between the inquirer, society, and the object of inquiry (e.g., the naturalcultural framework). We can also search for other values that can counteract objectionable consequences of past theoretical choices. Via such strategies, progress can be maintained and accelerated into the future.